Abstract
The structural dynamics and flexibility of cell membranes play fundamental roles in the functions of the cells, i.e., signaling, energy transduction, and physiological adaptation. The cyanobacterial thylakoid membrane represents a model membrane that can conduct both oxygenic photosynthesis and respiration simultaneously. In this study, we conducted direct visualization of the global organization and mobility of photosynthetic complexes in thylakoid membranes from a model cyanobacterium, Synechococcus elongatus PCC 7942, using high-resolution atomic force, confocal, and total internal reflection fluorescence microscopy. We visualized the native arrangement and dense packing of photosystem I (PSI), photosystem II (PSII), and cytochrome (Cyt) b6f within thylakoid membranes at the molecular level. Furthermore, we functionally tagged PSI, PSII, Cyt b6f, and ATP synthase individually with fluorescent proteins, and revealed the heterogeneous distribution of these four photosynthetic complexes and determined their dynamic features within the crowding membrane environment using live-cell fluorescence imaging. We characterized red light-induced clustering localization and adjustable diffusion of photosynthetic complexes in thylakoid membranes, representative of the reorganization of photosynthetic apparatus in response to environmental changes. Understanding the organization and dynamics of photosynthetic membranes is essential for rational design and construction of artificial photosynthetic systems to underpin bioenergy development. Knowledge of cyanobacterial thylakoid membranes could also be extended to other cell membranes, such as chloroplast and mitochondrial membranes.
Highlights
Oxygenic photosynthesis, the conversion of sunlight into chemical energy by higher plants, green algae, and cyanobacteria, underpins the survival of virtually all higher life forms
To study the native organization of cyanobacterial thylakoid membranes, we isolated thylakoid membranes from wildtype Synechococcus elongatus PCC 7942 (Syn7942) cells grown in liquid cultures through cell breakage by glass beads and step sucrose gradient centrifugation in the absence of detergents
Thylakoid membranes were collected from the 1.0–1.5 M fraction (Figure 1A) and were subjected to blue-native polyacrylamide gel electrophoresis (BN-PAGE) characterization of intrinsic photosynthetic complexes (Figure 1B)
Summary
The conversion of sunlight into chemical energy by higher plants, green algae, and cyanobacteria, underpins the survival of virtually all higher life forms. Oxygenic photosynthesis typically takes place in the specialized intracellular membranes, namely thylakoid membranes, analogous to higher plants. The cyanobacterial photosynthetic machinery embedded in thylakoid lipid bilayers typically consists of a series of membrane-integral multi-subunit complexes, including photosystem I (PSI), photosystem II (PSII), cytochrome (Cyt) b6f, and ATP synthase (ATPase) complexes. Cyanobacterial thylakoid membranes act as the site that harbors the components of respiratory electron transport chains, comprising type-I NAD(P)H dehydrogenase-like complex (NDH-1), succinate dehydrogenase (SDH), Cyt oxidase, and alternative oxidase
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